Limits...
Tracing the evolution of streptophyte algae and their mitochondrial genome.

Turmel M, Otis C, Lemieux C - Genome Biol Evol (2013)

Bottom Line: Our results indicate that important changes occurred at the levels of genome size, gene order, and intron content within the Zygnematales.In contrast, the two members of the Charales display an extremely conservative pattern of mtDNA evolution.Collectively, our analyses of gene order and gene content and the phylogenies we inferred from 40 mtDNA-encoded proteins failed to resolve the relationships among the Zygnematales, Coleochaetales, and Charales; however, they are consistent with previous phylogenomic studies in favoring that the morphologically complex Charales are not sister to land plants.

View Article: PubMed Central - PubMed

Affiliation: Institut de Biologie Intégrative et des Systèmes, Département de Biochimie, de Microbiologie et de Bio-Informatique, Université Laval, Québec, Canada.

ABSTRACT
Six monophyletic groups of charophycean green algae are recognized within the Streptophyta. Although incongruent with earlier studies based on genes from three cellular compartments, chloroplast and nuclear phylogenomic analyses have resolved identical relationships among these groups, placing the Zygnematales or the Zygnematales + Coleochaetales as sister to land plants. The present investigation aimed at determining whether this consensus view is supported by the mitochondrial genome and at gaining insight into mitochondrial DNA (mtDNA) evolution within and across streptophyte algal lineages and during the transition toward the first land plants. We present here the newly sequenced mtDNAs of representatives of the Klebsormidiales (Entransia fimbriata and Klebsormidium spec.) and Zygnematales (Closterium baillyanum and Roya obtusa) and compare them with their homologs in other charophycean lineages as well as in selected embryophyte and chlorophyte lineages. Our results indicate that important changes occurred at the levels of genome size, gene order, and intron content within the Zygnematales. Although the representatives of the Klebsormidiales display more similarity in genome size and intron content, gene order seems more fluid and gene losses more frequent than in other charophycean lineages. In contrast, the two members of the Charales display an extremely conservative pattern of mtDNA evolution. Collectively, our analyses of gene order and gene content and the phylogenies we inferred from 40 mtDNA-encoded proteins failed to resolve the relationships among the Zygnematales, Coleochaetales, and Charales; however, they are consistent with previous phylogenomic studies in favoring that the morphologically complex Charales are not sister to land plants.

Show MeSH

Related in: MedlinePlus

Gene repertoires of the streptophyte mitochondrial genomes examined in this study. The presence of a standard gene is indicated by a dark blue box and the presence of a pseudogene by a light blue box. The different colors on the left of the figure refer to gene distributions supporting distinct hypotheses concerning the sister group of land plants: orange, Zygnematales; brown, Coleochaetales + Zygnematales.
© Copyright Policy - creative-commons
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC3814193&req=5

evt135-F2: Gene repertoires of the streptophyte mitochondrial genomes examined in this study. The presence of a standard gene is indicated by a dark blue box and the presence of a pseudogene by a light blue box. The different colors on the left of the figure refer to gene distributions supporting distinct hypotheses concerning the sister group of land plants: orange, Zygnematales; brown, Coleochaetales + Zygnematales.

Mentions: Among the 16 charophycean and bryophyte mtDNAs examined in this study, the total number of standard genes ranges from 42 (in the hornwort Megaceros) to 71 (in Chlorokybus and the zygnematelean Closterium), with most genomes exhibiting between 65 and 71 genes (table 1). As in other charophycean mtDNAs, all protein-coding genes in the newly sequenced genomes were annotated using the standard genetic code, thus providing no evidence for RNA editing. The few genes that were lost from the mitochondrial genome during charophycean evolution code mainly for tRNAs (trn genes), ribosomal proteins (rps and rpl), and subunits involved in cytochrome c biogenesis (yej, also designated as ccm) (fig. 2). In land plant mtDNAs, the same categories of genes are prone to extinction (see fig. 2) (Adams et al. 2002; Knoop 2013). Certain mitochondrial genes were lost in a lineage-specific fashion, whereas others were lost in two or more lineages. Lineage-specific gene losses occurred at highest frequency in the Klebsormidiales and in the hornworts. The genes whose absence was recorded in multiple lineages are of special interest as they can be phylogenetically informative. In this context, we note that trnI(gau) is uniformly absent from the three bryophyte lineages and the Zygnematales, whereas rpl14 is missing from the bryophyte lineages, the Zygnematales and the Coleochaetales.Fig. 2.—


Tracing the evolution of streptophyte algae and their mitochondrial genome.

Turmel M, Otis C, Lemieux C - Genome Biol Evol (2013)

Gene repertoires of the streptophyte mitochondrial genomes examined in this study. The presence of a standard gene is indicated by a dark blue box and the presence of a pseudogene by a light blue box. The different colors on the left of the figure refer to gene distributions supporting distinct hypotheses concerning the sister group of land plants: orange, Zygnematales; brown, Coleochaetales + Zygnematales.
© Copyright Policy - creative-commons
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3814193&req=5

evt135-F2: Gene repertoires of the streptophyte mitochondrial genomes examined in this study. The presence of a standard gene is indicated by a dark blue box and the presence of a pseudogene by a light blue box. The different colors on the left of the figure refer to gene distributions supporting distinct hypotheses concerning the sister group of land plants: orange, Zygnematales; brown, Coleochaetales + Zygnematales.
Mentions: Among the 16 charophycean and bryophyte mtDNAs examined in this study, the total number of standard genes ranges from 42 (in the hornwort Megaceros) to 71 (in Chlorokybus and the zygnematelean Closterium), with most genomes exhibiting between 65 and 71 genes (table 1). As in other charophycean mtDNAs, all protein-coding genes in the newly sequenced genomes were annotated using the standard genetic code, thus providing no evidence for RNA editing. The few genes that were lost from the mitochondrial genome during charophycean evolution code mainly for tRNAs (trn genes), ribosomal proteins (rps and rpl), and subunits involved in cytochrome c biogenesis (yej, also designated as ccm) (fig. 2). In land plant mtDNAs, the same categories of genes are prone to extinction (see fig. 2) (Adams et al. 2002; Knoop 2013). Certain mitochondrial genes were lost in a lineage-specific fashion, whereas others were lost in two or more lineages. Lineage-specific gene losses occurred at highest frequency in the Klebsormidiales and in the hornworts. The genes whose absence was recorded in multiple lineages are of special interest as they can be phylogenetically informative. In this context, we note that trnI(gau) is uniformly absent from the three bryophyte lineages and the Zygnematales, whereas rpl14 is missing from the bryophyte lineages, the Zygnematales and the Coleochaetales.Fig. 2.—

Bottom Line: Our results indicate that important changes occurred at the levels of genome size, gene order, and intron content within the Zygnematales.In contrast, the two members of the Charales display an extremely conservative pattern of mtDNA evolution.Collectively, our analyses of gene order and gene content and the phylogenies we inferred from 40 mtDNA-encoded proteins failed to resolve the relationships among the Zygnematales, Coleochaetales, and Charales; however, they are consistent with previous phylogenomic studies in favoring that the morphologically complex Charales are not sister to land plants.

View Article: PubMed Central - PubMed

Affiliation: Institut de Biologie Intégrative et des Systèmes, Département de Biochimie, de Microbiologie et de Bio-Informatique, Université Laval, Québec, Canada.

ABSTRACT
Six monophyletic groups of charophycean green algae are recognized within the Streptophyta. Although incongruent with earlier studies based on genes from three cellular compartments, chloroplast and nuclear phylogenomic analyses have resolved identical relationships among these groups, placing the Zygnematales or the Zygnematales + Coleochaetales as sister to land plants. The present investigation aimed at determining whether this consensus view is supported by the mitochondrial genome and at gaining insight into mitochondrial DNA (mtDNA) evolution within and across streptophyte algal lineages and during the transition toward the first land plants. We present here the newly sequenced mtDNAs of representatives of the Klebsormidiales (Entransia fimbriata and Klebsormidium spec.) and Zygnematales (Closterium baillyanum and Roya obtusa) and compare them with their homologs in other charophycean lineages as well as in selected embryophyte and chlorophyte lineages. Our results indicate that important changes occurred at the levels of genome size, gene order, and intron content within the Zygnematales. Although the representatives of the Klebsormidiales display more similarity in genome size and intron content, gene order seems more fluid and gene losses more frequent than in other charophycean lineages. In contrast, the two members of the Charales display an extremely conservative pattern of mtDNA evolution. Collectively, our analyses of gene order and gene content and the phylogenies we inferred from 40 mtDNA-encoded proteins failed to resolve the relationships among the Zygnematales, Coleochaetales, and Charales; however, they are consistent with previous phylogenomic studies in favoring that the morphologically complex Charales are not sister to land plants.

Show MeSH
Related in: MedlinePlus